Figure 2. The stakeholders participating in Community Science initiatives.
The strategies listed above provide guidance in implementing prevention measures of different scales of society. Nevertheless, efficient prevention requires the close collaboration of not only partners within a certain program and scale, but partners across diverse scales. Information and expertise coming from grassroot science must be utilised to design and implement intervention plans on regional levels, which will feed into global frameworks collecting exemplary cases and efficient methods to be applied on other reservoir-pathogen systems in diverse policy environments.
Implementation strategies in different policy environments
When reviewing various EIDs, outbreaks and epidemics are often dealt with by different legal and economic frameworks depending on not only the scale they manifest on, but also on the newly infected host. Pathogens emerging in human communities, for instance, will come under the jurisdiction of public health and healthcare institutions, which has already resulted in the false interpretation that the EIDs are exclusively human diseases (79). Pathogens damaging livestock and crops are therefore seldom connected to those creating illness in humans, despite the anthropogenic drivers of their emergence (globalisation, climate change, international travel and shipping, human intrusion, etc.) and the socioeconomic impacts being the same in both severity and magnitude (18,46,51,80). Policy silos can further be observed in livestock diseases being addressed by food safety regulations and production management, while crop diseases being the concern of agricultural policies. Nevertheless, not only are the drivers of disease emergence the same, but pathogens colonising livestock and crops can increase the probability of emerging human diseases (45).
The One Health initiative considers all novel diseases a direct threat to human wellbeing and has been working to implement the One Health approach to medical, veterinary and wildlife disease management, urging for large scale, merged databases, expanding research focus to wild populations and reservoirs and preparing for future emergences (73,81,82). In line with these efforts, the DAMA calls for preventive intervention against all pathogens with a potential to emerge in human, livestock or crop populations. At the same time, this also means that prevention has to be planned and executed in three different policy environments. In the following sections, we will present the main focus points, target stakeholders and typical stumbling blocks of establishing LLs and CS programs in different policy infrastructures.
Human pathogens
Human diseases come under the deepest scrutiny and attract the most attention from authorities and the public alike. Nevertheless, there is major divergence between countries and regions in terms of healthcare infrastructure, pathogen diversity and sources of potential emergence. While temperate zone regions are more exposed to air-travel related infections being introduced (17), tropical and mediterranean areas have a higher potential for wildlife originated emergences (83). These patterns are then further complicated by climate change driving both species and human migration, providing opportunity for disease to expand their geographic, vector and host range. Chikungunya is an arboviral infection spread by the yellow fever mosquito (Aedes aegypti ) and was therefore referred to as a ‘tropical fever’ due its distribution area limited to that of its vector. However, 2010 saw the virus establish itself in the tiger mosquito (Aedes albopictus ) and produce autochthonous cases in Southern Europe (84), where it has since developed self-sustaining populations (85). Also an arbovirus moving from the Ae. aegypti to the Ae. albopictus , the ZIKA virus has seen its first local cases in Europe in 2019 (86) and is likely to threaten over a billion people with its recent range expansion (87). Finally, with the recent outbreaks of hepatitis of unknown aetiology (16) and the ongoing monkeypox outbreaks (88), it is clear that preparation for the barrage of human EIDs is unsustainable. The focus needs to shift towards prevention by launching multi-actor task forces handling emergence within a local and regional setting.
Living Labs preventing human pathogens
Preventing EIDs directly threatening human health will focus on the interfaces between human communities and identified reservoir populations where pathogens are expected to switch over to their new, susceptible host. Exposure will often be increased by living and working in close contact with wildlife (e.g. rural farming and hunting communities) and/or limited access to healthcare services coupled with improper maintenance of hygienic standards (e.g. urban poverty, marginalised communities) (1). Main focus points are to control and minimise the chances of pathogens switching over to humans, by either
targeting a specific host-pathogen system (e.g. Zika virus inAedes albopictus mosquitos) in which case we identify the stakeholders affected by this system, or
targeting people whose circumstances (living conditions, occupation, habits, etc.) supposedly place them at higher exposure (e.g. jobs during COVID-19 that do not carry a home office option), in which case we identify stakeholders connected to our target community.
From the groups outlined for LLs in general, the following actors should be considered relevant to preventing high risk human EIDs.
Public actors - government authorities addressing public health related matters, such as health services and public health authorities, national laboratories and epidemiological surveillance facilities, district health systems and district public health authorities and food safety institutions.
Private actors - private companies and organisations affected by potential emergence or connected to endangered communities. Relevant examples include pharmaceutical companies producing treatment or vaccines against the potential threat, travel agencies mapping international routes of concern, or software development and data management companies offering digital tools for tracking and monitoring human-pathogen interfaces.
Knowledge institutions - scientific institutions focusing on human pathogens, for instance epidemiology research laboratories, veterinary research groups working on reservoirs or vectors of the pathogen in question, and medical research institutions for human diseases.
Local citizens - community members should be involved in multi-actor task forces to represent local interest and expertise. Priority should be given to those already participating in CS programs or civil organisations, with an emphasis on engaging students and early career youth.
LLs handling human diseases will rely heavily on personal data regarding local workforce, financial status, access to health services, medical history and connectivity, it is therefore crucial to secure data protection and privacy. Furthermore, resources should be dedicated to communicating the process to the local community through paraprofessionals involved in the LL to establish solid working relationships and trust between the task force and locals. Relying on a collaborative foundation will not only facilitate implementation but also foster long-term engagement for maintaining preventive monitoring and screening.
Community Science programs preventing human pathogens
The focal point of disease prevention measures is engaging and working with communities directly exposed to the emergence of a novel pathogen. As described for LLs (see above), the target population for CS programs is identified (i) either through their contact with a particular reservoir or (ii) their circumstances making them susceptible to emergence of potential pathogens. Main focus points are to engage members of a community and initiate bidirectional communication channels between locals and researchers. On the one hand, prevention research relies heavily on knowledge of local habits and lifestyle, traditions, knowledge of reservoir behaviour and the interface between potential pathogens and community members. On the other hand, researchers can raise awareness on the lurking healthcare threat, establish educational and training programs, involve locals in the project and solidify collaboration by assigning leadership positions to paraprofessionals.
When planning recruitment within the community, factors to be considered include setting (e.g. rural vs. urban), occupation (local trade unions, commonalities between employment types, working conditions), socio-economic status (access to healthcare, level of education, household income) and cultural background (ethnicity, language, cultural habits and traditions, religion, etc.). Recruiting and training programs should be designed to be accessible and comprehensible for the target population, with a clear explanation of why they had been selected as participants.
Attention should be given to providing regular and thorough feedback on the process to all members of the community. Activities should be planned to ensure bidirectional flow of information: benefiting from community engagement should always be coupled with feedback sessions planned around delivering preliminary results, reflecting on experience of involved (academic and community) members and discussing potential impacts. This bidirectional discussion builds the trust and engagement required to establish long-term programs and networks, and builds a reliable network of non-scientific, local experts. Feedback should be constant during the actual sampling/collection to not only give back to the community, but to collect reflections and observations that can improve methods and communication strategies. A public facing website that is accessible for all stakeholders at all times is ideal, but regular newsletters or social media are popular ways to communicate effectively.
Contrary to LLs, CS programs are widely used to target infectious disease threats by monitoring bacterial pathogens polluting water bodies (89), preventing Lyme-disease (90), or monitoring viruses in urban environments (54). Methods and practices developed in previous programs should be implemented into newly established initiatives focusing on prevention.
Livestock pathogens
Diseases emerging in livestock have been just as impactful as those affecting humans directly. The past decades have seen an increase in both frequency and magnitude, with pandemics plaguing livestock across regions and continents (91,92). However, studies often focus on zoonoses rather than diseases affecting livestock directly, creating a lack of available information on pathogens of domesticated species (93). This bias in research is fueled by preferential funding for zoonotic diseases, which also manifests in lack of veterinary healthcare infrastructure, low efficiency or high priced medications, lapses in vaccination programs and knowledge discrepancies in breeders regarding diseases (94,95). Adding to the effects of this asymmetry in knowledge and research is the management of livestock diseases, which primarily aims to eliminate infected individuals from breeding stock, with extremely limited efforts dedicated to treatment development (96,97). Although there have been suggestions to introduce preemptive hunting strategies to avoid livestock being contaminated from wild populations (98), prevention still has a lot of ground to cover regarding livestock disease. This is further certified by the major economic effects livestock pandemics have, which add to the costs and damages caused by human EIDs. Foot and mouth disease of cattle resulted in up to 88% market value losses, affecting all actors along the cattle marketing chain in Uganda (99), while leading to the culling of 3.4 million animals during the UK epidemic (100). African Swine Fever has led to major economic losses in South-East Asia, and has triggered policy modifications linked to the emergence of SARS-CoV-2 (45,51). Avian influenza has not only led to dire losses in poultry production (80) but also to pandemic potential in humans (101). Therefore, in line with the One Health approach calling for integrated investigation of livestock, wildlife and human systems (102,103), the DAMA protocol calls for precautionary and preventive policies addressing livestock diseases.
Living Labs preventing livestock pathogens
Livestock disease will be of concern to different stakeholders than human pathogens, although a considerable overlap is to be expected. The drivers behind any preventive or managing intervention are mostly to maintain production and livelihood of breeders and production plants. Exposure will increase in free range breeding stocks and those housed partly in external enclosures, while outbreaks will be more likely to occur among high density stocks (104). Main focus points are to control and minimise the chances of pathogens switching over to livestock, by either
targeting a specific host-pathogen system (e.g. ASF in wild boar populations) in which case we identify the stakeholders affected by this system, or
targeting breeding facilities and game populations whose circumstances (housing conditions/distribution area, species, immediate surroundings etc.) supposedly place them at higher exposure (e.g. frequent encounters with (other) wildlife, limited access to veterinary/wildlife services, lack of knowledge regarding livestock/wildlife diseases, etc.), in which case we identify stakeholders connected to our target facilities.
From the groups outlined for LLs in general, the following actors should be considered relevant to preventing high risk livestock EIDs.
Public actors - government agencies involved in food safety, including national level institutions (e.g. Food Safety and Inspection Service (FSIS; US), Federal Institute of Risk Assessment (BIR; Germany), Austrian Agency for Health and Food Safety (AGES; Austria), Fish and Wildlife Department, as well as municipality level department of public health, agriculture, hunting and food safety.
Private actors - private companies and enterprises whose main activity is related to the livestock and/or game exposed to emergence. A few examples include farms, processing plants, hunting associations, suppliers and veterinary institutions providing vaccinations and medication. In case they are active in the area of potential emergence, companies offering digital tracking services recording movement, development and other data on individual animals, will also have valuable expertise in identifying interfaces and location of possible intervention to reduce encounters between livestock and reservoirs.
Knowledge institutions - research groups targeting the livestock and game pathogen under investigation as well as those conducting research in livestock and wildlife vaccination, treatment, methods to increase production and environmental effects on stock yield. Furthermore, veterinary science is also a key stakeholder contributing to knowledge on transmission, morbidity and mortality, and to potential direction of treatment and/vaccine development.
Local citizens - required expertise will be found among individual farmers and workers at breeding and processing facilities, as well as hunters, who not only hold valuable insights regarding animal behaviour and diseases but are also directly exposed to any emerging pathogen due to their constant close contact with the breeding stock and wildlife.
LLs handling livestock and game diseases must always consider that, contrary to those dealing with human pathogens, they will have dual priorities of preventing emergence and maintaining or even increasing production. As livelihood of most stakeholders is closely connected to yield of breeding stocks and game populations, tools such as culling or restricting stock size, increasing hunting bag size or applying targeted hunting should be used with extraordinary caution to establish long-term feasibility of prevention methods.
Community Science programs preventing livestock pathogens
CS programs targeting livestock diseases are far less common than those addressing human pathogens, since the community affected by them is much smaller and consists almost exclusively of citizens working in livestock breeding or processing and hunters. Whether a CS initiative is designed to target (i) a particular pathogen and the livestock or game exposed to it or (ii) breeding stocks and game populations whose circumstances make them susceptible to emergence of potential pathogens, the initiative will be of interest to a narrower community of local experts.
Main focus points are to engage breeding experts and individual hunters that work in close contact with animals and are aware of the day-to-day issues and conditions of a breeding/processing facility or a particular hunting area. Livestock experts will be able to identify interfaces between the stock and wildlife accurately, while hunters will be familiar with movement and behavioural patterns of game and potential reservoirs, as well as population sizes and demography.
When planning recruitment strategies, a close collaboration is required with the management of the breeding facility(s) for efficient study design and institutional encouragement to participate. It is also necessary to align interests of larger breeding enterprises and small-scale, local farmers to ensure the homogeneity of data collected. An additional opportunity lies in designing studies for the general audiences, targeting those that are active outdoors and therefore have occasional encounters with wildlife. Recruiting and training programs should be designed to be accessible and comprehensible for the target population, with a clear explanation of why they had been selected as participants.
To avoid unnecessary investment, planning must always consider existing data collected by breeders and hunters, as both institutions collect particular types of data on a permanent basis. This is available either from government institutions overseeing wildlife management or private breeders keeping their own records, both subject to restricted access. Similarly, feedback sessions and reports have to be targeted to both citizen participants and the institutional board overseeing the stock in question, which can alter the format of the feedback.
CS programs have been introduced into research focusing on wildlife health surveillance (75) as well as monitoring invasive vector species (55). Studies have also used CS methods to target diseases plaguing wildlife and livestock simultaneously (105) and to identify shortcomings of policies addressing foot and mouth disease (106).
Crop pathogens
Crop pathogens are commonly the most neglected EIDs since they pose no immediate health risk to humans and therefore mostly manifest in indirect effects due to decreased production. Crop pathogens have typically been addressed by palliative efforts eliminating them from the cultivated plant stock (107,108) or later applying defence priming against known crop diseases (109). Macroscopic pests of crops have a longer history of defence strategies, as microscopic pathogens had only been discovered to coincide with plant diseases in the late XIXth century and named as a cause decades later (110). Initial research focus gradually shifted from epidemiology towards control and founded commercial disease control with a wide range of bactericide, fungicide and virucide treatments, as well as extensive gene-modification research breeding resistant crops lineages (110). Although without such protection measures, losses in crop production could increase five-fold in Europe (111), it has now become clear that global demand as well as changing climate and globalised trade have subjected crops to EIDs unmanageable by current measures. Additional to coconut yellow disease and wheat stem rust described above, tomatoes are plagued by rapidly spreading, diverse viral diseases (112), grapevine downey mildew has spread from Europe and now threatened vineyards worldwide (113), and the Fusarium incarnatum-equiseti species complex had invaded leafy vegetable crops in novel European areas (114). Although still treated as an agricultural and production issue, more studies are connecting plant diseases to the larger context of EIDs (115–117). In line with this, evidence shows that plant pathogens follow similar evolutionary trajectories to those described in the Stockholm Paradigm, for instance Phytoplasmas using common receptors distributed across several insects that serve as vectors to infect plants (118,119).
Although the overlap between plant and human pathogens is presumably negligible, the effect of emerging plant pathogens on global food security is devastating, which justifies their inclusion within the preventive measures of the DAMA protocol.
Living Labs preventing crop pathogens
Crop pathogens will be of interest to stakeholders quite different than described for human and livestock diseases, with smaller overlaps. However, some similarities will exist between motivation for preventing crop and livestock EIDs, namely the drive to maintain production and yield of crops. Also, exposure will increase in those planted in the vicinity of wild areas, with large scale monocultural fields being at elevated risk of epidemics and outbreaks. Additionally, growing similar species in close spatial or temporal proximity may further increase the chances of transferring pathogens from one to the other (120). Main focus points are to control and minimise the chances of pathogens switching over to crop plants, by either
targeting a specific host-pathogen system (e.g. phytoplasma in their vector insects) in which case we identify the stakeholders affected by this system, or
targeting areas or particular crops whose circumstances (distribution area, species, immediate surroundings etc.) supposedly place them at higher exposure (e.g. large areas bordering natural habitats, limited access to agricultural and control services, lack of knowledge regarding crop diseases, etc.), in which case we identify stakeholders connected to our target areas or species.
From the groups outlined for LLs in general, the following actors should be considered relevant to preventing high risk crop EIDs.
Public actors - government ministries involved in agricultural services, including national level institutions (e.g. National Institute of Food and Agriculture (NIFA; US), Federal Ministry of Food and Agriculture (Germany), Federal Ministry of Agriculture (Austria), as well as municipality level departments of public health, agriculture, and food safety.
Private actors - private companies and enterprises whose main activity is related to the crop and/or area exposed to emergence. A few examples include farms, plantations, suppliers and agricultural institutions providing protection methods. In case they are active in the area of potential emergence, companies offering digital mapping services recording distribution, density, species composition, and other data in high resolution, will also have valuable expertise in identifying interfaces and location of possible intervention.
Knowledge institutions - research groups involved in agri-food sciences relating to the emergent threat, working on control measures such as resistant lineages, pesticides, defence priming techniques, and ways of increasing production, as well as those studying the distribution and genetic mapping of the pathogen in question.
Local citizens - required expertise will be found among individual farmers and workers working with investigated crops or in relevant areas, as well as the general public visiting natural areas in the vicinity of the cultivated plants. Both will have direct insights into the manifestation and the distribution of the disease and will be able to point out significant interfaces between crops and wild reservoirs or hosts.
A further similarity to LLs handling livestock and game diseases, those addressing crop diseases must also aim to prevent emergence and maintain or increase production at the same time. Additionally, since current control measures hold off substantial losses in production, prevention measures must accommodate ongoing treatment protocols. Finally, different regions will often have very different infrastructure on cultivated areas, which will have a significant influence on the potential prevention plans and their feasibility.
Although particular plant pathogens have been addressed by multi-actor approaches targeting pathogens such as cassava viruses (121), the Living Lab approach is still to be utilised to its full potential in preventing and controlling emerging crop diseases.
Community Science programs preventing crop pathogens
Unlike in livestock diseases, CS programs tend to have a more thorough representation in crop disease studies. This is mainly due to the economic drivers of controlling crop pests as well as the larger community of farmers and general public that is able to contribute. Whether a CS initiative is designed to target (i) a particular pathogen and the cultivated species exposed to it or (ii) crops whose circumstances make them susceptible to emergence of potential pathogens, the initiative will be of interest to a wider audience than in the case of livestock diseases.
Main focus points are to engage farmers, cultivation experts and individuals living or frequenting endangered areas, who will possess the knowledge on crop and reservoir species as well as specifics on the area of cultivation. Training programs should primarily focus on developing skills to identify particular wild plant species and recognize signs of infection, which will also be useful in tracking invasive species in the future. Recruiting and training programs should be designed to be accessible and comprehensible for the target population, with an additional educational role in raising awareness about food security issues and conscientious consumer behaviour. Depending on the setting of the study, a long-term return can be encouraging participants to grow produce at home, thereby increasing green areas and increasing self-sustaining households.
The benefit of CS programs in crop health has been established regarding potato diseases (122) and identifying main threats of maize and soybean in the Amazon region (123). Additionally, data collected by a relatively small number of expert citizens has been demonstrated to be highly accurate (124), which makes CS programs very promising for implementing the DAMA protocol.
Conclusions
The EID crisis represents one of the largest threats to modern lifestyle, endangering human health, food security, economic and societal systems. Isolated institutions dealing with various manifestations of EIDs have thus far been unsuccessful in stopping the wave of newly emergent pathogens. The SP provides a comprehensive evolutionary framework, which replaces current, false characterization of EIDs with clear predictions. The DAMA protocol provides a general step-by-step plan for constructing preventive interventions targeting emergent pathogens before the onset of an outbreak. This paper focuses on the final step of implementing evolutionary theory into preventive policies considering scales and policy environments.
Global, regional and local scales require precise conceptualization and the introduction of adequate transdisciplinary methods to gather all relevant knowledge and expertise, and create feasible, cost-efficient intervention plans. Global integration of the DAMA protocol into existing frameworks is crucial to provide useful guidelines to regional and national institutions; this is described in the Prevent-Prepare-Palliate (3P) framework. Regional scales addressing EID threats are to introduce the widely tested approach of Living Labs, which can be seen as multi-actor platforms delivering solutions co-created by various stakeholders. Their application to infectious disease threats will be a unique contribution which has significant potential of dealing with diverging interests. Finally, local scales would benefit from a wide-range of Community Science initiatives targeting affected populations directly and the assistance of local experts on various host-pathogen systems. Although each method is most suitable for their particular scale, it is crucial that all of them operate in close collaboration with each other, circulating knowledge from the grassroots towards institutions. The key to disease prevention is ongoing monitoring that engages local experts, citizens, as well as relevant decision-makers in bidirectional communication.
Another important step towards more effectively controlling the EID crisis is eliminating the barriers among human health care, wildlife health care, livestock health care and crop health care. The current lack of a unifying scientific understanding of health issues results in divergent policies providing palliative and perhaps preparatory solutions, none of which is efficient or sustainable in the face of accelerating EIDs. By understanding the common underlying evolutionary drivers, predictions can be adjusted appropriately across the board for human, livestock and crop diseases, and prevention can be implemented onto existing infrastructures and legal environments.
Our advancements in technology have brought with them novel threats in the shape of EIDs. Climate change and globalisation have changed the evolutionary trajectory of diseases as we know them, it is therefore inevitable to change our approach to global health security and shift our focus from reactive approaches to those moving up the infection timeline towards prevention.